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Red de Revistas Científicas de América Latina y el Caribe, España y Portugal
© 2014
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas 13 (5): 498 -
505
ISSN 0717 7917
www.blacpma.usach.cl
Artículo Original | Original Article
498
Screening for extracts with insect antifeedant properties
in native plants from central Argentina
[Evaluación de la actividad antialimentaria de insectos en extractos de plantas nativas del centro de Argentina]
Soledad DEL CORRAL
1
, Georgina N. DIAZ-NAPAL
1
, Mariano ZARAGOZA
1
, María C. CARPINELLA
1
,
Gustavo RUIZ
2
and
Sara M. PALACIOS
1
1
Fine Chemical and Natural Products Laboratory, School of Chemistry, Catholic University of Córdoba.
2
Herbarium Marcelino Sayago, School of Agricultural Science, Catholic University of Córdoba.
Av. Armada Argentina 3555, Córdoba, Argentina
Contactos | Contacts:
Sara M. Palacios
- E-mail address:
sarapalacios@ucc.edu.ar
Abstract:
Ethanol extracts obtained from aerial parts of 64 native plants from Central Argentina were tested for their insect antifeedant
activity against
Epilachna paenulata
(Coleoptera: Coccinellidae) by choice test. Extracts derived from
Achyrocline satureioides
(Asteraceae),
Baccharis coridifolia
(Asteraceae),
Baccharis flabellata
(Asteraceae),
Ruprechtia apetala
(Polygonaceae) and
Vernonanthura
nudiflora
(Asteraceae), showed more than 97% inhibition of the feeding of
E. paenulata
at 100
g/cm
2
. These active extracts were further
evaluated for their effectiveness against
Spodoptera frugiperda
(Lepidoptera: Noctuidae). All these extracts except for that derived from A.
satureioides, negatively influenced the feeding behavior of
S. frugiperda
at 100
g/cm
2
.
Keywords:
Native plants to Argentina; insect antifeedants;
Vernonanthura nudiflora
;
Baccharis flabellata
;
Baccharis coridifolia
;
Ruprechtia apetala
;
Achyrocline satureioides
.
Resumen:
Se evaluaron los extractos etanólicos obtenidos de las partes aéreas de 64 plantas de la región Central de Argentina, como
antialimentarios de insectos mediante ensayos de elección, contra
Epilachna paenulata
(Coleoptera: Coccinellidae). Los extractos derivados
de
Achyrocline satureioides
(Asteraceae),
Baccharis coridifolia
(Asteraceae),
Baccharis flabellata
(Asteraceae),
Ruprechtia apetala
(Polygonaceae) y
Vernonanthura nudiflora
(Asteraceae) mostraron mas de 97% de inhibición de la alimentación de
E. paenulata
a 100
g/cm2. Estos extractos fueron posteriormente evaluados en su efectividad contra
Spodoptera frugiperda
(Lepidoptera: Noctuidae). Todos
ellos, con
excepción del extracto de
A. satureioides
, afectaron negativamente el comportamiento alimentario de
S. frugiperda
a 100
g/cm2.
Palabras clave
:
Plantas nativas de Argentina; antialimentarios de insectos;
Vernonanthura nudiflora
,
Baccharis flabellata
;
Baccharis
coridifolia
;
Ruprechtia apetala
;
Achyrocline satureioides
Recibido
| Received:
June 12, 2013
Aceptado en versión corregida | Accepted in revised form:
September 10, 2014
Publicado en línea | Published online:
September 30, 2014
Declaración de intereses | Declaration of interests:
This work was supported by the Catholic University of Córdoba, FONCYT, Grant Numbers: BID 1728 OC/AR. PICT 33593
and PICTO CRUP 6-31396. SDC and GDN gratefully acknowledge receipt of a fellowship from CONICET.
Este artículo puede ser citado como / This article must be cited as:
S del Corral, GN Diaz-Napal, M Zaragoza, MC Carpinella, G Ruiz, SM Palacios. 2014. Screening for
extracts with insect antifeedant properties in native plants from Central Argentina.
Bol Latinoam Caribe Plant Med Aromat
13(5): 498 – 505.
del Corral et al.
Insect antifeedant activity of Argentinian native plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/499
INTRODUCTION
Chemical control of pest insects has given rise to
several
problems
including
the
pollution
of
the
environment by insecticide residues (de Vlaming
et
al.
, 2004), the selection of resistant pest populations
(Storer
et al.
, 2012),
the negative side effects on
beneficial parasites and predators (Cordero
et al.
,
2007)
and the deleterious effects on human health (de
Jong,
1991, Sulak
et
al.
,
2005).
It
is
therefore
necessary to design efficient insect control agents
presenting reduced environmental consequences (Diaz
Napal
et al.
, 2009).
Plants synthesize a wide array of compounds
that are involved in plant-insect interactions. Such
compounds of secondary metabolism as alkaloids,
terpenoids, phenols, flavonoids, steroids, etc. confer
some
resistance
against
phytophagous
insects
(Carpinella
et al.
, 2002; González-Coloma
et al.
,
2002; Urzúa
et al.
, 2010a; Urzúa
et al.
, 2010b; Urzúa
et al.
, 2011; Céspedes
et al.
, 2013). These compounds
act as antifeedant and toxic substances as well as
growth
regulators
affecting
several
physiological
processes of insects (González-Coloma
et al.
, 2002).
In this context, we are studying the insecticidal
potential of the flora of Central Argentina (Palacios
et
al.
,
2007, Palacios
et
al.
,
2009),
searching
for
environmentally-friendly pesticides. As a result of this
ongoing study, we have identified several plants as
sources of efficient pest controllers (Defagó
et al.
,
2006, Diaz Napal
et al.
, 2009, Diaz Napal
et al.
, 2010,
Palacios
et al.
, 2010, Defagó
et al.
, 2011). In this
report, we examine the insect antifeedant properties of
another group of 64 plants from Central Argentina
against
Epilachna paenulata
, as part of this program
for the selection of highly active plant species for
natural insecticide development.
E.
paenulata
Germar
(Coleoptera:
Coccinellidae) is a phytophagous insect that affects
species from the Cucurbitaceae family, which was
extensively used in our laboratory as model insect for
insecticide studies (Diaz Napal
et al.
, 2010).
The
results were then confirmed testing the most active
extracts in another pest insect: the fall armyworm
Spodoptera frugiperda
(Lepidoptera: Noctuidae). This
insect comprises a pest of economic importance for
basic grain production
and for many other crops in
North, Central and South America (Wyckhuys &
O’Neil, 2006). Being the main corn pest in Brazil and
in Argentina (Tavares
et al.
, 2009),
S. frugiperda
has
developed
resistance
against
many
synthetic
insecticides (Tomquelski & Martins, 2010)
and against
transgenic BT-maize (Storer
et al.
, 2012).
MATERIALS and METHODS
Plant material
Plants
were
collected
in
the
hills
of
Córdoba,
Argentina, from November 2010 to December 2011.
Voucher
specimens
have
been
deposited
in
the
“Marcelino Sayago” Herbarium of the School of
Agricultural Science, Catholic University of Córdoba
and were authenticated by the botanist, Gustavo Ruiz.
Plants were selected according to their availability and
accessibility and emphasing those for which there was
no
information
about
their
activity
or
chemical
contents. The vegetative material was air-dried at
room temperature, crushed and extracted by 48 h
maceration
with
ethanol.
Yields
of
each
viscous
extract, obtained after solvent removal, were expressed
as percentage weight of air-dried plant material.
Insects
E. paenulata
and
S. frugiperda
larvae were obtained
from a laboratory colony, reared on a natural diet of
Cucurbita maxima
Duch. leaves and artificial diet
(Céspedes
et al.
, 2000), respectively. The insects were
maintained in a growth chamber at 24 ± 1º C and 70-
75% relative humidity, with a photoperiod of 16/8 h
light-dark cycle and periodically renewed with field
specimens (Diaz Napal
et al.
, 2010).
Test solution preparation
Ten mg of each extract were dissolved in 1 mL of
acetone immediately before the corresponding assay.
Feeding choice assay
Two cotyledon leaves from a
C. maxima
seedling were
placed in a Petri dish; a glass disk with two 1 cm
2
diameter holes was placed on top. A third-instar
E.
paenulata
larva was placed equidistant from both a
treated and an untreated leaf disk, with 10
l of test
solution
and
10
l
of
acetone,
solvent
control,
respectively. The insect was allowed to feed for 24 h.
Ten replicates were run for each test. In the case of the
assays against
S. frugiperda
, two circular sections of
Lactuca sativa
seedling were placed in a Petri dish. A
third-instar
S. frugiperda
larva was placed equidistant
from both a treated (with 10
l of test solution) and an
untreated (with 10
l of acetone, solvent control) leaf
disk, and allowed to feed until 50 percent of the food
was
eaten.
The
relative
amounts
(recorded
in
del Corral et al.
Insect antifeedant activity of Argentinian native plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/500
percentages from 0 to 100) of the treated and untreated
substrate areas eaten in each test were estimated
visually by dividing the food area into imaginary
quarters. An antifeedant index (AI) was calculated as
[1- (T/C)] x 100 (Diaz Napal
et al.
, 2009), where T
and C represent consumption on treated and untreated
food, respectively.
A rank for each of the most active plants was
estimated considering an index (I
n
) calculated for that
plant extracts by the following equation:
I
n
= y
n
. AI (
E. paenulata
) . AI (
S. frugiperda
)
where I
n
is the rank of the species n, y
n
is the yield
extract of plant n base on 100 g of plant material, and
the AI is the antifeedant index of extract of plant n at
100
g/cm
2
for each insect. The plant extract with the
highest I
n
is the most active one and consequently
received the lowest rank number (Rank = 1), with
lower I
n
receiving consecutive rank numbers (Rank >
1).
Statistical analysis
Results from feeding choice assays were analyzed for
statistical significance using the Wilcoxon signed
ranks test.
RESULTS and DISCUSSION
The
feeding
inhibition
properties
of
each
extract
obtained from the 64 plant species were evaluated in a
choice feeding assay against
E. paenulata
. Most of the
species were native to our environment although some
of
them
(
Cotoneaster
glaucophylla
,
Dipsacus
fullonum
,
Marrubium vulgare
,
Melissa
officinalis
and
Podranea ricasoliana
) are in fact naturalized. The
results of this screening are presented in Table 1.
Table 1
Insect antifeedant activity of extracts from native plants against
Epilachna paenulata
.
Plant species
AI(%)
a
Achyrocline satureioides
(Lam.) DC.
97.14
Achyrocline tomentosa
Rusby
27.00
Aloysia citriodora
Palau
66.90
Aloysia gratissima
(Gill.& Hook.) Tronc.
75.70
Ambrosia elatior
L.
-7.20
Amphilophium cynanchoides
(DC.) L.G. Lohmann
21.00
Angelphytum aspilioides
(Griseb.) H. Rob.
92.26
Argemone subfusiformis
G. B. Ownbey
91.80
Baccharis artemisioides
Hook. & Arn.
76.60
Baccharis coridifolia
DC.
98.20
Baccharis flabellata
Hook. & Arn.
97.00
Baccharis salicifolia
(Ruiz & Pav.) Pers.
27.00
Bidens pilosa
L.
57.14
Capparis atamisquea
Kuntze
26.00
Condalia microphylla
Cav.
63.50
Cortaderia rudiuscula
Stapf
-2.20
Cotoneaster glaucophylla
Franch.
4.30
Croton lachnostachyus
Baill.
5.00
Dipsacus fullonum
L.
8.71
Dolichandra unguis-cati
(L.) L.G. Lohmann
5.00
Dysphania ambrosioides
(L.) Mosyakin & Clemants
2.00
Eryngium horridum
Malme
46.40
Eupatorium hookerianum
Griseb.
29.00
del Corral et al.
Insect antifeedant activity of Argentinian native plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/501
Eupatorium viscidum
Hook. & Arn.
42.00
Flourensia campestris
Griseb.
85.16
Gomphrena pulchella
Mart.
77.50
Grindelia pulchella
Dunal
96.12
Jarava ichu
Ruiz & Pav.
1.50
Jodina rhombifolia
(Hook. & Arn.) Reissek
0.00
Ligaria cuneifolia
(Ruiz & Pav.) Tiegh.
54.90
Lippia turbinata
Griseb.
37.25
Lithrea molleoides
(Vell.) Engl.
11.00
Mandevilla laxa
(Ruiz & Pav.) Woodson
-83.00
Marrubium vulgare
L.
71.30
Melinis repens
(Willd.) Zizka
52.50
Melissa officinales
L.
42.00
Microliabum candidum
(Griseb.) H. Rob.
29.00
Minthostachys verticillata
(Griseb.) Epling
56.41
Morrenia brachystephana
Griseb.
64.13
Ophryosporus charrua
(Griseb.) Hieron.
51.23
Pavonia aurigloba
Krapov. & Cristóbal
34.00
Podronea ricasoliana
(Tanfani) Sprague
80.00
Porlieria microphylla
(Baill.) Descole, O’Donell & Lourteig
75.00
Pterocaulon alopecuroides
(Lam.) DC.
95.90
Pyrostegia venusta
(Ker Gawl.) Miers
55.00
Ruprechtia apétala
Wedd.
97.75
Schizachyrium condensatum
(Kunth) Nees
-18.00
Senecio madagascariensis
Poir.
67.36
Senecio vira-vira
Hieron.
78.00
Senna aphylla
(Cav.) H.S. Irwin & Barneby
39.00
Sida rhombifolia
L.
87.80
Solanum argentinum
Bitter & Lillo
26.00
Solanum palinacanthum
Dunal
39.20
Solanum sisymbriifolium
Lam.
80.30
Sphaeralcea bonariensis
(Cav.) Griseb.
14.00
Spharalcea cordobensis
Krapov. (mutant)
49.00
Tagetes minuta
L.
85.00
Tripodanthus flagellaris
(Cham. & Schltdl.) Tiegh.
67.00
Verbesina encelioides
(Cav.) Benth. & Hook. f. ex A. Gray
0.00
Vernonanthura nudiflora
(Less.) H. Rob. f. nudiflora
99.00
Vernonia mollissima
Hook. & Arn.
47.00
Viguiera tucumanensis
(Hook. & Arn.) Griseb. var. tucumanensis
25.40
Wedelia glauca
(Ortega) O. Hoffm. ex Hicken
93.80
Zanthoxylum coco
Hook.f. & Arn.
83.00
Azadiracthin
b
100.00
a: data represent the mean of ten replicates.
b: reference natural insecticide at 4
g/cm
2
Those extracts that possess an AI between 50-75%
were previously classified as moderate antifeedants
(Hassanali & Lwande, 1989). Only those with values
greater than 75% were considered to have high values.
According to this criteria, 20% of the plant extracts
showed
moderate
antifeedant properties
(13/64
=
20%) against
E. paenulata
at 100
g/cm
2
,
whereas 13
extracts (13/64 = 20%) had activity between 75% and
95% and only 7 extracts (7/64 = 11%) exhibited an
AI
superior to 95%. This last group is composed of the
extracts
derived
from
Achyrocline
satureioides
,
Baccharis coridifolia, Baccharis flabellata, Grindelia
del Corral et al.
Insect antifeedant activity of Argentinian native plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/502
pulchella,
Pterocaulon
alopecuroides,
Ruprechtia
apetala,
and
Vernonanthura nudiflora.
The rest of the
plant extracts were divided between the non-active
(27/64 = 42%)
and the phagostimulant extracts with
negative AI (4/64 = 6%).
Within the group with the greatest antifeedant
activity, the most active ones were also tested against
S. frugiperda
, a polyphagous pest that is possibly
more tolerant to allelochemicals
due to its ability to
detoxify xenobiotics (Ali & Agrawal, 2012). Four
extracts also showed high antifeedant activity against
S. frugiperda
,
B. coridifolia
and
V. nudiflora
were the
most active (Table 2). The effectiveness of these
extracts suggests that they can be used as sources
of
natural antifeedants to control harmful pests. These
results also suggest that these extracts could contain
highly active secondary metabolites. If we assume that
such activity is due to a single metabolite and taking
into account
that these compounds do not normally
exceed 10% of the extract, the results suggest that
active ingredients would exert the antifeedant effect at
a concentration approximately of 10
g/cm
2
. This
level of activity make these compounds especially
promising antifeedants, as compared with the vast
majority of the plant antifeedants which are effective
only at doses greater than 20
g/cm
2
(Koul, 2005).
The
well-known
antifeedants
azadirachtin
or
meliartenin (Carpinella
et al.
, 2006) have equivalent
activities against
E. paenulata
and
S. frugiperda
at 4
and 1
g/cm
2
, respectively.
Table 2
Most active plant extracts against
Epilachna paenulata
and
Spodoptera frugiperda
AI (%)
Plant species
Yield (g%)
E. paenulata
S. frugiperda
Rank
a
Achyrocline satureioides
4.5
97.14
33.60
5
Baccharis coridifolia
2.2
98.20
91.22
3
Baccharis flabellata
7.5
97.00
80.36
2
Ruprechtia apetala
1.9
97.75
81.30
4
Vernonanthura
nudiflora
7.2
99.00
98.61
1
a: for rank calculation, see Materials and Methods section.
In anticipation of the application of these
extracts to control insects in domestic or organic
agriculture, we propose to categorize each extract as
an insect control product taking into account the
antifeedant activity as well as the extract yield of each
species. With this aim in mind, we established a rank
of the most active extracts, using their yields and their
activity on both insects, which are listed
in Table 2.
V.
nudiflora
,
B. flabellata,
B. coridifolia, R. apetala
and
A. satureioides
had ranks from 1 to 5, respectively.
Based on the aforementioned analysis, it is
clear that extracts from
V. nudiflora, B. coridifolia
and
B. flabellata
constitute the most promising insect
control products.
V. nudiflora
(Asteraceae) is a herbaceous plant
with blue-purple flowers that is considered a weed in
many crops. Neither antifeedant reports nor bioguided
studies have been found in the literature for its
ethanolic extract. Aerial parts of
V. nudiflora
furnished
glaucolides A and B,
flavonoids,
hirsutinolide and
cadinanolides derivatives (Bardón
et al.
, 1992). The
antifeedant activity of
V. nudiflora
could be attributed
to glaucolide A, which has previously been reported
as a feeding deterrent against lepidopteran larvae
(Burnett Jr
et al.
, 1974).
B. coridifolia
(Asteraceae) is a low-growing
woody shrub known as “mio-mio”. This plant has an
extensive distribution that includes the north-east,
center and north of Argentina. No reference about
antifeedant activity was found for this species. As far
as we know, this is the first report on this matter,
although the plant is toxic to livestock (Rizzo
et al.
,
1997). The toxins of
B. coridifolia
are macrocyclic
trichothecenes, including roridin A, D, and E and
verrucarin
A
and
J (Rizzo
et
al.
,
1997).
The
trichothecins in this plant are generally considered to
be produced by entophytic fungi that live within the
plant,
although
some
soil
microbes,
primarily
Myrothecium roridum
and
M. verrucaria
, may also
make them, they are no longer considered to be
absorbed by the plants (Busam & Habermehl, 1982)
but rather produced within them.
From
the
aerial
parts
of
B.
flabellata
(Asteraceae),
neo-clerodane
diterpenoids
such
as
flabeloic
acid,
5,10-seco-clerodane
diterpenoid
derivative (Saad
et al.
, 1988),
2,19;15,16-diepoxy-
del Corral et al.
Insect antifeedant activity of Argentinian native plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/503
neo-clerodan-3,13,14-trien-18-oic acid, 15,16-epoxy-
5,10-seco-clerodan-1
(10),2,4,13(16),14-pentaen-18,
19-olide and 15,16-epoxy-neo-clerodan-1,3,13(16),14-
tetraen-18,19-olide were isolated (Juan Hikawczuk
et
al.
, 2002). Some related neo-clerodanes isolated from
different
species
have
been
reported
as
effective
antifeedant compounds (Muñoz
et al.
, 1997, Bremner
et al.
, 1998, Cifuente
et al.
, 2002) although this plant
was not previously reported as antifeedant against
insects.
R.
apetala
(Polygonaceae),
known
as
“manzanito del campo”, is a small tree with pale pink
flowers. Not many activities have been reported for
the
ethanolic
extract,
however
a
potent
anticholinesterase inhibitory effect has been found
(Carpinella
et al.
, 2010). This property could be
connected with the anti-insect activity observed in this
screening.
A. satureiodes
(Asteraceae) (common name
“marcela”) is a low-growing shrub with a woody base
or suffrutex with grayish leaves. Infusions from this
plant are used today in southern Brazil, Paraguay and
Argentina for the treatment of different illnesses.
Bactericidal
properties
of
this
species
have
been
demonstrated (Joray
et al.
, 2011a, Joray
et al.
, 2011b),
however,
no
information
about
its
antifeedant
properties has been reported.
In conclusion, the plants with good ranking,
especially
V. nudiflora
,
B. coridifolia
and
B. flabellata
may be considered as potential insect control materials
for
different
agricultural
practices,
due
to
their
potencies and yields. It could also be highly advisable
to study both the responsible compounds for the
antifeedant effect and their mechanisms of action.
ACKNOWLEDGEMENTS
This work was supported by the Catholic University of
Córdoba,
FONCYT,
Grant
Numbers:
BID
1728
OC/AR. PICT 33593 and PICTO CRUP 6-31396.
SDC and GDN gratefully acknowledge receipt of a
fellowship from CONICET. We thank Julie Mariano
for revising the English language and two anonymous
reviewers for helpful suggestions.
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